Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

Abstract

Eusocial societies present a Darwinian paradox, yet they have evolved independently in insects, mole-rats and symbiotic shrimp. Historically, eusociality has been thought to arise as a response to ecological challenges, mediated by kin selection, but the role of kin selection has recently been questioned. Here we use phylogenetically independent contrasts to test the association of eusociality with ecological performance and genetic structure (via life history) among 20 species of sponge-dwelling shrimp (Synalpheus) in Belize. Consistent with hypotheses that cooperative groups enjoy an advantage in challenging habitats, we show that eusocial species are more abundant, occupy more sponges and have broader host ranges than nonsocial sister species, and that these patterns are robust to correction for the generally smaller body sizes of eusocial species. In contrast, body size explains less or no variation after accounting for sociality. Despite strong ecological pressures on most sponge-dwellers, however, eusociality arose only in species with non-dispersing larvae, which form family groups subject to kin selection. Thus, superior ability to hold valuable resources may favour eusociality in shrimp but close genetic relatedness is nevertheless key to its origin, as in other eusocial animals.

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

“…(d) Social structure Social structure was estimated using a variation of the eusociality index [38], calculated as E ¼ 1 2 (2 Â Q)/N, where N is colony size and Q is the number of reproductive females (sensu [22,23]). The eusociality index (E) incorporates both a colony's size and its reproductive skew making the simplifying assumption that all breeding individuals contribute equally to offspring production.…”

“…Not only has eusociality evolved independently at least four times [22][23][24] in the group of approximately 45 West Atlantic (Gambarelloides) species [25], but reproductive skew varies continuously among species with different social structures: (i) eusocial species live in colonies with a single or a few 'queens' and a few to hundreds of non-breeding workers; (ii) communal species live in groups with multiple breeding pairs, typically with equal ratios of adult males and females and (iii) pair-living species live in sponges with a single breeding pair per sponge [23,26]. All species within the Gambarelloides groups live obligatorily in sponge canals, and therefore appear to face similar ecological constraints on social living.…”

“…Third, we measured sexual dimorphism based on female and male allometries between chela length and body size. Lastly, we calculated the eusociality index [39] for each species as a measure of reproductive skew (sensu [23]). We compared these metrics among species of Synalpheus to test three key predictions, namely that as reproductive skew increases, (i) reproductive conflict among females would increase, (ii) females would be expected to develop larger weapons and (iii) sexual dimorphism would decrease.…”

The Right Tools for the Job: Cooperative Breeding Theory and an Evaluation of the Methodological Approaches to Understanding the Evolution and Maintenance of Sociality

“…Thus far, the majority of comparative studies have focused on terrestrial taxa which has resulted in many great advancements in the field (Brown, 1974;Arnold and Owens, 1998;Boomsma, 2009;Riehl, 2013). However, marine organisms are relatively understudied in terms of comparative work, which is unfortunate as they offer a rich diversity of social organization and varied ecological niches and life-history strategies with which to explore the various hypotheses of social evolution and maintenance (McLaren, 1967;Gowans et al, 2001;Duffy and Macdonald, 2010; FIGURE 2 | Approximate number of articles published on each of the major hypotheses using comparative, observational and experimental methodologies. Abbreviations are: Kin, Kinship; Monog, Monogamy; LH, Life-history; EC, Ecological Constraints; BoP, Benefits of Philopatry.…”

“…The size, structure and composition of these groups can vary both within and between species, from pair-bonding monogamous partners (Kleiman, 2011;Servedio et al, 2013) to large and highly complex societies exhibiting social hierarchies and division of labor (Duffy and Macdonald, 2010;Nandi et al, 2013). Such variation in social structure is intriguing as it suggests that there may be a great diversity of underlying social, ecological or life history factors that influence the evolution of stable groups and their maintenance over many generations.…”